166 I Litteratura Serpentium, 1994, Vol. 14, Nr. 6

Poto 1: ursinii eriwanensis. Poto: Jan Bergman.

Poto 2: . Vrouwtjes. Females. Poto: Jan Bergman. Some notes on the genus Vipera / 167

SOME NOTES ON THE GENUS VIPERA (SERPENTES: : ) IN ANATOLIA, TURKEY

By: Jan Bergman, RMmansb. 27, 14556 Norsborg, Sweden and Mikael Norstrom, Mickel­ bergsv. 78, Hagersten, Sweden.

English corrections by Mark Wootten.

Contents: Introduction - Observations - Pelias-group - Rhinaspis-group - Lebetina-group - Xanthina-group - Acknowledgements - Literature. * * *

INTRODUCfION

Since the late 1980's, the Turkish herpetofauna in general, and the genus Vipera in parti­ cular have been studied relatively well (Nilson et al., 1988, 1990; Billing et al., 1990; Schatti et al., 1991). During 8 field trips, we have visited large parts of Anatolia and made numerous observations both on the Anatolian genus Vipera as well as on the sympatric -fauna. Here we present this, with additional data on altitude of occurrence, habitat preference and observations on captive reproduction. We also give some information on several new localities inhabited by various of Vipera, based on reports from local inhabitants. These people were asked to identify various snake species from colour photographs. The photographs highlighted differences between species that are easily confused ( e.g. Coluber ravergi.eri with members of the Xanthina-group, Coluber nummifer with the Lebetina­ group, and Coronella austriaca with the Pelias-group ). Whenever there was any uncertainty in the identification, it was rejected. The occurrence of Coluber ravergi.eri and Coluber nummifer appears to be a good indication for the presence of, Vipera xanthina and Vipera lebetina, respectively. The same applies to Coronella austriaca and Vipera ursinii (Bergman, in prep.). The co-occurrence of a specific viper and its harmless image can be regarded as Batesian mimicry.

OBSERVATIONS

Pelias-group (Merem, 1820).

• Vipera ursinii eriwanensis (Reuss, 1933). We have observed specimens of this taxon during April and May, between Asbuga and Catac (province of Kars ), at 2000-2200 m above sea level. Other snake species observed in this area are Coronella austriaca austriaca and Natrix tessellata tessellata. In May 1985 a shed skin of this species was found northwest of Aladag (province Kars ). Several other suitable habitats for this species can be found in adjacent provinces 168 I Litteratura Serpendum, 1994, Vol. 14, Nr. 6

;,, - -~ -'.:,f. ,,. Foto 3: Vipera transcaucasiana. Jong mannetje die een duizendpoot heeft uitgebraakt. A juvenile male has vomitted a big scolopender. Foto: Jan Bergman.

Foto 4: Coluber nummifer. Vertoont batesiaanse mimicry met Vipera lebetina. Batesian mimicry to Vipera lebetina. Foto: Jan Bergman. Some notes on the genus Vipera I 169

(Agri, Erzerum, Tuncelli, and Sivas), but the occurrence of Vipera ursinii eriwanensis in those regions has not been acknowledged. These habitats are similar to those observed near Aladag (volcanic rocks and subalpine meadows). Some of these potential habitats, however, are damaged by extensive sheep grazing. Extensive grazing not only causes changes in micro-habitat, but the disappearance of insect foodplants as well. This leads to low insect densities, which, in tum, cause a reduction of insectivores ( e.g. lizards) because of a shortage of food. The lack of lizards and insects, important prey items to Vipera ursinii eriwanensis, will have a negative effect on the survival of this species, in the future. Captive reproduction has been unsuccessful so far. This may be caused by the low body weight of the females, due to an increase in metabolic rate under too warm and stressful captive conditions.

• Vipera kaznakovi (Nikolsky, 1909). This medium-sized viper is locally known as 'kantra'. It can be found in Northeast Anatolia between Hopa and (province of Artvin) (Norstrom, 1988). In this region the habitats are dominated by a rich vegetation, because of the high precipitation level. However, small microhabitats consisting of stony areas and bare earth can be found in this area as well. These patches are favoured by Vipera kaznakovi, especially when there is some Rubus ssp. and Pteridium aquilinum-vegetation present. Vipera kaznakovi has been observed, at an altitude of 800m above sea level, within a stone and bush mixed habitat situated south of Hopa (Bergman, 1991 ). In Turkey, no previous observations of Vipera kaznakovi have been made at this altitude (Billing et al., 1990; Bergman, 1991). However, this species has recently been observed at altitudes up to 1000m in former Soviet territory (Kurdajavtsev & Mamet, 1989). Sympatrical ( co-occurring) snake species observed in the Hopa-area are: Natrix megalocephala, Natrix natrix scutata, Coronella austriaca austriaca and Elaphe longissima longissima. In captivity, Vipera kaznakovi has a gestation period varying between 90-96 days and litter size may be 3-12 neonates. Females normally have a reproductive cycle every other year. This is, however, highly depending on the availability of prey after gestation. Schweiger (1992) placed Vipera kaznakovi in the Rhinaspis-group, based on biochemical characteristics. However, we are of the opinion that some of the caucasian taxa belong to a group of their own, which forms a possible intermediate group between the Pelias­ and Rhinaspis-groups. Species such as Vipera kaznakovi, Vipera dinniki, Vipera ponti.ca and Vipera barani may belong to such an intermediate group.

Rhinaspis-group (Bonaparte, 1834)

• Vipera transcaucasiana (Boulenger, 1913). This species, previously considered a of Vipera ammodytes, is now regarded as a distinct species (Hermann et al., 1987). It displays the upturned snout, just like Vipera ammodytes, but it is patterned more like Vipera aspis. The recognition of Vipera transcaucasiana is entirely based on biochemical characteristics. We have found this viper in three different places. It seems to occur along most of the northwest coast of Asia Minor. Vipera transcaucasiana is common around Amasra, east of Zonguldak (province of Adapazari). Here it was found in secondary habitat resulting from bush fires on limestone slopes in macchia-meadows. The elevation of the collecting 170 I Litteratura Serpentium, 1994, Vol. 14, Nr. 6

site is 300 m above sea level. In this area Vipera transcaucasiana was found co-occurring with Coluber caspius and Elaphe longissima longissima. Within the Coruh valley (province of Artvin) about 300 m above sea level, this viper lives in terrain with sunspotted stone openings in heavy bush vegetation. Here Vipera transcaucasiana was found co-occuring with Natrix natrix scutata, Coluber ravergi,eri and Coluber schmidti. In the province of Sivas it can be found in open bush vegetation with extensive rock formations, up to 1650 m above sea level. Sympatric observed here are Natrix tes­ sellata tessellata, Coluber caspius, and Typhlops vermicularis. In a summary of the distribution of the genus Vipera in Turkey (Nilson et al 1988), the occurence of Vipera transcaucasiana in the province of Kars is not included. However, the presence of Vipera transcaucasiana in this area was already stated in 1986 (Nilson and Andren, 1986). According to our experience, it is quite unlikely that this species is an inhabitant of the Kars province because of the generally high altitude and the different (unsuitable) climate. The distribution of this species seems to follow the <;oruh river valley and its tributaries, starting from Georgia. Vipera transcaucasiana seems to prefer secondary enviroments ( clear felled areas, areas affected by fires, areas grazed by cows, etc), where the undergrowth is low and rich. If the undergrowth is dense it is confined to the open areas. We have found that this species is sensitive to intensive grazing by sheep and goats. Specimens from the Taurus mountains (Eiselt and Baran 1970), South Konya (Topla­ kat, pers. comm.), and Konya (Nilson and Andren, 1986) may belong to a: separate taxon, distinct from the northern and central populations. Based on similarities with Greek specimens, Nilson and Andren (1986) regard these as Vipera ammodytes meridio­ nalis. The southernmost observation of this taxon is made Northwest of Silifke, in South Turkey (Manteuffel, 1993). However, no conclusive evidence for the occurrence of this species this far south exists. Because of the similarity of this species with some colour morphs of Coluber ravergi,eri, this observation might well be a misidentification ( see also: Franzen and Schmidtler, 1993). The dorsal ground colour in males tends to change geographically from lime gray in west, lead gray in central and brown gray in east Turkey. A juvenile specimen from Kase Dag (province of Sivas) regurgitated a large millipede. Many recently caught specimens were heavily infected with endoparasites (Nematodes and Cestodes). Only two captive reproductions were observed. In one couple, the male started courtship 31 days after its first spring moult, copulation followed 6 days later. Eighty-four days later the female gave birth to 11 viable young. In another couple, copulation took place at the end of may. 4 Juveniles were born at the end of August.

Lebetina-group (Linnaeus, 1758)

• Vipera lebetina obtusa (Dwigubskij, 1832). The members of this group are included in the re-introduced genus Macrovipera, by some authors. A single specimen was found dead on a road close to Nurdag in the province of Adana. The collecting site is located in a highly cultivated area. In this area Coluber jugularis was found as well. Another case of mimicry is observed in this species and its colubrid image Coluber nummifer. Some notes on the genus Vipera I 171

Foto 5: Vipera wagneri. Mannetje. Male. Foto: Jan Bergman.

Foto 6: Vipera albizona. Vrouwtje met tekening gelijk aan vrouwtjes van V. wagneri en V.xanthina. Female shows similar pattern to both V. wapneri and V.xanthina females. Foto: Jan Bergman. 172 I Litteratura Serpentium, 1994, Vol. 14, Nr. 6

Xanthina-group (Gray, 1849)

• Vipera xanthina, the Ottoman viper (Gray, 1849). This species has been observed in the hills north of the ruin-town Efesus (province of Izmir). Vipera xanthina, like many other vipers, frequently inhabits the stone walls that enclose cultivated areas. Other snakes observed in Efesus were Typhlops vermicularis, Eirenis modestus, Coluber jugularis, Coluber najadum najadum, and Coluber rubriceps rubriceps Vipera xanthina, the Ottoman viper, has been bred successfully in captivity. The success, however, is highly depending on age and size of the females. The number of offspring varies between 2-9 juveniles.

• Vipera wagneri (Nilson and Andren, 1984 ). This beautiful species has been observed by us in May 1989, within the valley of the Aras-river (Bergman 1992), at an altitude of 1600-1850 meters above sea level. After the site of its discovery had been revealed by Jager et al. (1988), the population of Vipera wagneri was drastically reduced by the activities of (local) snake catchers, who sold the snakes to collectors. An intense captive breeding programme is necessary to reduce the strain on the wild population, because of the constant demand for new specimens by private collectors and institutions (Bergman, in press). Elaphe hohenackeri, Elaphe quatuorlineata sauromates, Coluber ravergi,eri, and Natrix tessellata tessellata were observed sympatrically within the region of Aras. Vipera wagneri inhabits a habitat of volcanic boulders, just like Vipera raddei which only lives a few kilometers away in the Aras valley. Vipera raddei, however, seems to prefer a drier enviroment. The gestation period of 13 females bred by us varied between 103-107 days with an offspring of 4-8 juveniles (Bergman in press). Under ideal conditions, females can reach maturity at an age of 2 years.

• Vipera albizona (Nilson, Andren and Flardh, 1990). This viper was found by us in May 1990, at the -locality ( = the locality where the specimens of the species' first description originate from) in the province of Sivas. The habitat consisted of volcanic rocks, at an altitude of 1850-1900 meters. The populations of this species are fragmented and isolated; the population-density seems to be very low. Co-occuring with Vipera albizona at the type-locality were Coluber ravergi,eri and Eirenis modestus. According to local shepherds Vipera ursinii can be found here as well. One female, which reproduced in 1990, did not eat enough during 1991 to attain a body weight suitable for another successful reproduction. This may imply a 2 year, or perhaps even longer, reproductive cycle. One captive female is known to have given birth to six young in October. Schatti et al. (1991) consider Vipera albizona to be conspecific with Vipera xanthina. We are, however, of the opinion that it is more closely related to Vipera wagneri. Specimens of Vipera albizona, observed by us, show very clear morphological differences with Vipera xanthina, Vipera bommulleri and Vipera wagneri.

• Vipera raddei (Boettger, 1890). This species, described earlier as Vipera xanthina raddei by Mertens (1952), seems to have been confused with Vipera wagneri from Tuzluca (Province Kars, Bergman, in press b ). Some notes on the genus Vipera / 173

Foto 7: Coluber ravergieri. Vertoont batesiaanse mimicry met Vipera xanthina. Batesian mimicry to Vipera xanthina. Foto: Jan Bergman.

1 Foto 8~ Vipera raddei 'kurdistanica • Jong exemplaar geboren in gevangenschap. Juvenile born in captivity. Foto: Jan Bergman. 174 I Litteratura Serpentium, 1994, Vol. 14, Nr. 6

We have found Vipera raddei at Mount Ararat at an altitude range of 1550-1700 meters above sea level. Within the volcanic boulder habitat at Mnt. Ararat the following sympatric snake species were observed: Eryx jaculus familiaris, Coluber ravergieri, Coluber schmidti, Natrix sp, Elaphe hohenackeri, Elaphe quatuorlineata sauromatus. In some locations aggregations of over 100 specimens have been observed just below the snowline (Mulder, pers. comm.). The polymorphism in populations of this species, existing in certain areas in North­ West Iran is probably _caused by historical climatological and geological reasons. The members of these populations are described by Nilson and Andren (1986) as a distinct subspecies, Vipera raddei kurdistanica. Two other, closely related, taxa, Vipera latifii (polymorphic) and Vipera albicornuta (monomorphic) are considered to be separate species by the same authors. None of the specimens observed in areas in southern Turkey and former differ from the Turkish subspecies kurdistanica in colour, but the pattern may be polymorphic. This species is therefore considered monotypic by Schatti et al. (1991). According to Vinegar (1974) and our own observations, pregnant females of other snake species that are kept under suboptimal temperature conditions during embryogenesis can produce offspring with pattern aberrations that closely resemble the polymorphic pattern of Vipera raddei. It is well known that specimens of a population that lives near the periphery of the species distribution, often have a reduced gene flow compared with the central population, which have a constant influx of 'new' blood. Within other small viper populations e.g. and Vipera dinniki polymorphism also occurs frequently. The gestation period for one female from Yuksekova was in progress for 99 days when three young were born.

ACKNOWLEDGEMENTS

We have crossed many areas with the following persons: Jan Wihman (Skansen Alcva­ riet), Mats Hoggren (Department of Genetics, Uppsala University), Leif Westrin (Stock­ holm), Jimmy Thidell (Norsborg), Borje Flardh (Tumba and the Natural History Museum in Gothenburg) and Jan Petterson (Vadstena). We are grateful to all of these persons for field assistance. We are very grateful to the Family Aydin (Sarikamis), for native help with language, hospitality and guidance. We must also give gratitude to the people in Ovacic who helped us in many ways, during our two fieldtrips to that area. The same applies to the people in the village of Karabag.

LITERATURE

Bergman, J., 1991. Juvenilt pamingsbetende hos Vipera kaznakovi. Snoken 4(21): 16-17 (In swedish with english summary).

---, 1992. Ein erster Fund einer abnormalen, runden pupille bei Vipera wagneri (Nilson und Andren, 1984). Sauria 14(1): 33.

---, In press a. Hasselsnoken, Coronel/a austriaca, en indikator och imitator, levande i amexistens med Peliasgruppen ? Med synpunkter pll sUiktet Viperas 6vrigartkomplex, och dess samexistens med andra Colubridformer. Snoken (In swedish with english summary). Some notes on the genus Vzpera / 175

---, In press b. Erfarenhet av Vi.pera wagneri i natur och terrarium. Snoken (In sweetish with english summary).

Billing, H., G. Nilson & U. Sattler, 1990. Vi.pera pontica sp. n. a new viper species in the kaznakovi group (Reptilia, Viperidae) from northeastern Turkey and adjacent transcaucasia. Zool. script. 19(2): 227-231.

Franzen, M. & J.F. Schmidtler, 1993. Erwinderung zu: 'Bericht ilber Reptilienfunde in der Tiirkei' von Dietmar Manteuffel. Salamandra 29(1): 92-95.

Hermann, H.W., U. Jager, G. Nilson & C.G. Sibley, 1987. First step towards a iochemically based reconstruction of the phylogeny of the genus Vipera. Proc. 4th ord. Gen. meet. S.E.H., Nijmegen, 195-200.

Jager, U., A Teynie & D. Fuchs, 1988. Morphological characterization of Vi.pera wagneri Nilson and Andren 1984 (Reptilia: Viperidae) with first description of the males. Bonn. Zool. Beitr. 39(2/3): 221-228.

Kudajavtsev, S.V. & S.V. Mamet, 1989. Terestrial snakes of the Sovietunion. The snake 21: 29-35.

Manteuffel, D., 1993. Bericht iiber Reptilienfunde in der Tiirkei. Salamandra 28(3/4): 223-230.

Mertens, R., 1952. Amphibien und Reptilien aus der Tiirkei. Rev. Fae. Sci. Univ. Istanbul (Ser. B) 17: 41-75.

Nilson, G. & C. Andren, 1986. The mountain Vipers of the middle East: The Vi.pera xanthina complex (Reptilia, Viperidae). Bonn. Zool. Monogr. 20: 1-90.

---, C. Andren & B. Flardh, 1988. Die Vipern der Tiirkei. Salamandra 24: 215-247.

---, C.Andren & B. Flardh, 1990. Vipera albizona, a new mountain Viper from Central Turkey, with comments on isolation effects of the Anatolian 'Diagonal'. Amphibia-Reptilia 11: 285-294.

Norstrom, M., 1988. Erfarenhet av den Kaukasiska viperan Vipera kaznakovi i Turkiet. Fauna och Flora 83: 26-33 (In swedish).

Schweiger, M., 1992. Die Europaische Hornotter Vi.pera ammodytes (LINNAEUS 1758). Teil 1: Systematik, okologie und Lebenweise. Herpetofauna 14(77): 11-22.

Schatti, B., I. Baran & H. Sigg, 1991. Rediscovery of the Bolkar Dagh viper: morphological variation and systematic implications on the 'Vipera xanthina complex'. Amphibia-Reptilia 12: 305-327.

Vinegar, A, 1974. Evolutionary implications of temperature induced anomalies of development in snake embryos. Herpetologica 30: 72-74.